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Journal of Agricultural Technology 2015 Vol. 11(8): 2547-2561
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ISSN 1686-9141
In Silico Identification, Classification And Expression Analysis Of Genes
Encoding Putative Light-Harvesting Chlorophyll A/B-Binding Proteins In
Coffee (Coffea Canephora L.)
Cao Phi Bang1*, Tran Thi Thanh Huyen2
1
Biotechnology Research Center, Faculty of Natural Sciences, Hung Vuong University
Department of Plant Physiology and Application, Faculty of Biology, Hanoi National
University of Education
2
Cao P.B. and Tran T.T.H. (2015). In Silico identification, classification and expression analysis
of genes encoding putative light-harvesting chlorophyll a/b-binding proteins in coffee (Coffea
canephora L.). Journal of Agricultural Technology 11(8): 2547-2561.
The light-harvesting proteins bind to chlorophyll a/b and transfer light energy to photosynthetic
reaction centre. These proteins also play a major role in photoprotection and abiotic stress
tolerance in many plants. By using in silico methods, a total of 28 genes encoding putative light
harvesting complex (LHC) have been identified in coffee (Coffea cenaphora) genome. Most of
putative LHC deduced proteins possess the Chloroa_b-bind (PF00504) conserved domain.
Based on phylogeny analysis, these coffee LHC genes have been classified into many groups,
including photosystem (PSI, PSII), LHC-related and light-inducible genes. Both PSI and PSII
groups were divided into six subgroups, respectively (A1-A6) and (B1-B6) All the subgroups
contain one member each, except B1and B3 subgroup which contain multiple genomic loci
(five members). The B2 and B4 are single locus subgroups in C. cenaphora but they are
multiple genomic loci in both A. thaliana and rice. In contrast, B3 subgroup contains four genes
in C. cenaphora but only one member in A. thaliana. In general, the transcripts of most of
coffee putative LHC genes are abundant in leaves and perisperm but weakly or not detectable in
roots. In addition, most of the genes are expressed in pistil. The coffee early light-inducible
protein encoding genes are strongly expressed in all the investigated tissues.
Key words: coffee , chlorophyll a/b binding protein, light-harvesting complex proteins, gene
identification, gene classification, gene expression, in silico analysis.
Introduction
Plants absorb light energy for photosynthesis by using two types of lightharvesting complexes (LHC-I and LHCII). The light harvesting proteins bind to
chlorophyll a/b and transfer light energy to photosynthetic reaction centre
(Jansson, 1994). Besides plants, the light-harvesting proteins, present in
different taxa including cyanobacteria, purple bacteria and green sulphur
bacteria, exhibit low sequence similarity although some structural similarity
*
Corresponding Author: Cao Phi Bang, Email: [email protected]
2547
can be observed (Green, 2001). In higher plants, the LHC proteins constitute a
large family of proteins which consists of chlorophyll a/b-binding proteins
(CABs), high light-induced proteins (HLIPs), early light-induced proteins
(ELIPs), the psbS subunit of photosystem II (psbS), and stress-enhanced
proteins (SEPs) (Jansson, 1994).
The structure of LHC proteins from many different species such as algae
and higher plants contain three transmembrane helices together with
characteristic LHC motif (ExxxxRxAM) (Green and Kuhlbrandt, 1995). LHC
proteins play a major role in light absorption and photoprotection (reviewed in
(Neilson and Durnford, 2010). The LHC proteins of PSII (LHCB proteins),
involved in the stomatal response to abscisic acid, are important for drought
tolerance of A.thaliana (Liu et al., 2013; Xu et al., 2012). Among the LHCrelated proteins, the early light-induced proteins were the most studied. These
proteins play a key role in photoprotection and abiotic stress response in a large
number of species such as A. thaliana (Hutin et al., 2003), Rhododendron
catawbiense (Peng et al., 2008), grape vine and pea (Berti and Pinto, 2012) and
tea (Li et al., 2013). Recently, thanks to public
availability of
the genome sequences, the LHC gene family has been genome-wide identified
an analyzed in some plant species such as brown alga (Dittamiet al., 2010), A.
thaliana and rice (Umate, 2010).
Coffee is one of the most important trade beverages with over 2.25 billion
cups consumed a day (Denoeud et al., 2014). The coffee seeds contain many
classes of biochemical compounds such as flavonoids, phenolics, alkaloids,
terpenoids and rich in stimulant caffeine (Leroy et al., 2006).This plant is an
economically important crop in more than 60 countries in South and Central
America, Asia, and Africa with over 11 million ha of plantation (Denoeud et
al., 2014). Currently, Coffea arabica and C. canephora are two major varieties
of the coffee cultivated worldwide. C. canephora, which represents
approximately 38% of coffee production (Vieira et al., 2006) is the diploid
species (2n = 2x = 22). This species is one of the parents of the allotetraploid
C. arabica (2n = 4x = 44 chromosomes) which was derived from hybridization
between C. canephora and C. eugenioides (Lashermes et al., 1999). The
genomic sequence of C. canephora which has been completely sequenced in
2014, is a powerful resource for helping the research on main traits such as
quality, yield, protection against pests, and abiotic stress tolerance to face
climatic changes (Denoeud et al., 2014).The analysis of LHC encoding genes in
coffee is particularly relevant since coffea is mainly grown in tropical and
subtropical regions under relatively high intensities of light.
Objectives: This work aimed to genome-wide identify the putative LHC
genes in C. cenaphora genome by using in silico methods. In addition, the
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Journal of Agricultural Technology 2015 Vol. 11(8): 2547-2561
classification and expression of these LHC genes were analyzed.
Material and methods
Identification of LHC from coffee genomic sequences
Based on the coffee genome (http://coffee-genome.org/) (Dereeper et al.,
2015), an extensive research was performed for identifying all members of the
LHC family. Firstly, the LHC sequences of A. thaliana (Umate, 2010) were
used as queries to perform blastp (Altschul et al., 1997) against coffee genome
database with an e-value of le-10. Secondly, the selected coffee genes were
used as queries for BLAST search on the coffee genome for identifying the
coffee paralogs that had been excluded by their dissimilarity to the Arabidopsis
orthologs. Finally all candidate sequences were submitted to domain research
by using the Pfam software (http://www.sanger.ac.uk/software/pfam) (Finn et
al., 2014).
Sequence analysis and construction of the phylogenetic tree
The molecular weight, theoretical pI and GRAVY (grand average of
hydropathy) of putatives sequences were calculated by the PROTPARAM tool
(http://web.expasy.org/protparam/) (Gasteiger et al., 2003). Subcellular
localization analysis of the deduced amino acids was performed using TargetP
1.1 Server (http://www.cbs.dtu.dk/services/TargetP/) (Emanuelsson et al.,
2007). The transmembrane protein topology was predicted by using the
PSIPRED Server (http://bioinf.cs.ucl.ac.uk/psipred/) (Buchan et al., 2013).
Phylogenetic analyses were conducted using MEGA version 5 (Tamura et
al., 2011). Complete coffee LHC predicted proteins were aligned using the
MAFFT server (http://mafft.cbrc.jp/alignment/server/) (Katoh and Standley,
2013) then phylogenetic trees was constructed by using the Maximum
Likelihood method with 1000 bootstraps.
Gene expression analyses
The relative LHC gene expression log10(RPKM) (Reads Per Kilobase of
transcript per Million fragments mapped) values were obtained from (Denoeud
et al., 2014).
2549
Results and Discussions
Identification of the HLC genes in coffee genome
The LHC protein sequences from C. cenaphora have been identified by
using the BLASTP programme with queries from A. thaliana (Umate, 2010).
Then, the second blastp was performed against coffee genome using selected
coffee genes as queries. A total of twenty-eight full-length genes encoding
putative LHC proteins have been identified. When these predicted proteins
were analyzed by using Pfam, only 24 of the 28 candidate sequences exhibit
Chloroa_b-bind (PF00504) conserved domain. The four remaining sequences
(CcSEP1, CcSEP2, CcHOP and CcHOP2) were grouped with A.thaliana and
rice orthologs on phylogenetic tree (Figure 1). The LHC gene family is smaller
in coffee compared to A. thaliana and rice families which have 30 and 29 genes
respectively.
The coffee putative LHC genes have a size ranging from 510 to 4057
nucleotides in genomic full-length. Except of six, all of the genes exibit intron
(from 1 to four introns). Their deduced full-length protein sequences range
from 122 to 330 amino acids. Among them, CcOHP has a smallest size with
molecular mass of 13.39kDa while CcChla/b-like has a biggest size with
molecular mass of 36.35kDa. Theoretical pI values of Coffee LHCs fluctuate in
a wide range from 4.53 to 9.91, with 21 acidic and seven basic LHCs. The LHC
encoding gene family has been genome-wide indentified in A.thaliana and rice
(Umate, 2010). The characteristics of coffee LHC are in agreement with
orthologs of A. thaliana and rice. AtOHP (locus At5G02120) and OsOHP1
(LOC_Os05g22730) are also the smallest LHC protein with 110 amino acids
(MW of 12,01 kDa) and 113 amino acids (MW of 12,11 kDa), respectively.
Theoretical pI values of coffee LHCs is consistent with pI range of A. thaliana
(4.61~11.51) and rice (4.14~12.82) (Umate, 2010). Transmembrane helix
predictions using PSIPRED server (Buchan et al., 2013) show that major
(17/28) of coffee LHCs have three helices. Two sequences exhibit one helix
(CcOHP and CcOHP2) when the remaining ones (including CcSEP1 and
CcSEP2) contain two helices. Subcellular localization analysis of the deduced
amino acids using TargetP 1.1 Server (Emanuelsson et al., 2007) suggests that
majority of LHC proteins are present in chloroplast but one member
(CcLHCB1.1) is probably targeted to mitochondria.The predicted localization
of the four additional ones is ambiguous.
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Journal of Agricultural Technology 2015 Vol. 11(8): 2547-2561
Table 1. Inventory and characteristics of the LHC genes identified in C. canephora
Genomi Protei
Intron
c
n
MW
Subgrou Locus
T s
Gen
full
full
(kDa pI
p
name
M numbe
lenght lenght )
r
(bp)
(aa)
CcLHCB3
Cc00_g127
18.5 4.5
LHCB3
510
169
2
0
.1
90
1
8
CcLHCB3
Cc00_g348
18.5 4.5
LHCB3
510
169
2
0
.2
70
1
8
Cc02_g191
14.5 9.7
CcSEP1
SEP1
2242
143
2
3
80
6
8
Cc02_g217
27.7 8.7
CcLHCB6 LHCB6
999
262
3
1
20
9
8
CcLHCB1
Cc02_g335
25.8 9.9
LHCB1
1841
229
3
2
.1
60
5
1
Cc03_g043
20.2 8.9
CcELIP
ELIP
806
191
2
2
00
3
3
Cc04_g164
27.7 6.1
CcLHCA4 LHCA4
1002
252
3
2
10
1
1
CcLHCB1
Cc05_g096
25.7 5.3
LHCB1
802
242
2
1
.2
50
0
2
Cc05_g099
29.3 6.4
CcLHCA3 LHCA3
1257
273
3
2
30
8
3
CcLHCB3
Cc05_g127
28.4 5.0
LHCB3
1012
263
3
2
.3
20
0
3
Cc06_g014
31.1 5.5
CcLHCB4 LHCB4
1087
286
3
1
60
1
9
Cc06_g023
13.3 9.8
CcOHP
OHP
596
122
1
2
40
9
0
Cc06_g124
28.6 5.5
CcLHCA6 LHCA6
1761
260
3
4
80
2
2
CcLHCB3
Cc07_g002
18.5 4.5
LHCB3
510
169
2
0
.4
60
7
3
Cc07_g161
22.6 5.2
CcSEP2
SEP2
1471
209
2
1
20
8
5
Cc08_g113
28.9 5.0
CcLIL
LIL
2526
261
2
2
60
7
2
CcLHCB1
Cc09_g090
28.1 5.4
LHCB1
795
264
3
0
.3
30
7
4
Cc09_g095
28.5 5.9
CcLHCB2 LHCB2
1851
265
3
3
00
7
6
CcLHCB1
Cc09_g090
28.2 5.6
LHCB1
795
264
3
0
.4
10
8
7
CcLHCB1
Cc09_g090
28.2 5.2
LHCB1
795
264
3
0
.5
20
2
7
Cc09_g020
26.2 5.8
CcCHLA1 LHCA1
1334
244
3
1
10
4
4
Subcellul
ar
location
Other
Other
C
C
M
C
C
C
C
C
C
C
C
Other
C
C
C
C
C
C
C
2551
Table 1 continued
Genomi
c
full
lenght
(bp)
Protei
Intron
n
MW
Subcellula
Subgrou Locus
T
s
Gen
full
(kDa pI
r
p
name
M numbe
lenght )
location
r
(aa)
CcChla/b CHLa/b- Cc10_g0014
36.3 6.3
4057
330
3
5
C
-like
like
0
5
2
CcLHCA
Cc10_g0419
28.9
LHCA5
1639
268
6.6 3
5
C
5
0
3
Cc10_g1189
28.4 6.7
CcPsbS
PsbS
2312
271
3
3
C
0
0
6
Cc10_g1518
20.0 9.3
CcOHP2 OHP2
3125
188
1
1
C
0
6
3
CcLHCB
Cc10_g1621
31.0 5.3
LHCB5
1632
289
3
5
C
5
0
0
4
CcLHCA
Cc11_g1691
31.4 6.2
LHCA2
1340
287
3
2
Other
2
0
7
1
MW : molecular weight, TM : transmembrane helix, pI : isoelectrical point, C: chloroplast, M:
Mitochondria
Classification of coffee LHC genes
The coffee LHCs were classified based on phylogenetic tree which was
constructed from LHC proteins of three species including rice, A.thaliana and
Coffee (Figure 1). The results of phylogeny analysis show that the coffee LHCs
are divided into many groups, the chlorophyll a/b-binding proteins of PSI lightharvesting, the chlorophyll a/b-binding proteins of PSII light-harvesting, the
LHC-related proteins and light-inducible proteins. The first group contains six
members classified into six subgroups (A1-A6), with one gene in each
subgroup like in A. thaliana and rice. These predicted protein sequences are not
so different in size (ranging from 244 to 287 amino acids) and in theoretical pI
(ranging from 5,52 to 6.60). The second group includes 14 genes divided into
six subgroups (B1-B6). Similarly to A. thaliana and rice, the B5 and B6
subgroups have single locus gene while B1 subgroup has multiple genomic
loci. The size of coffee B1 subgroup is similar (five members) to Arabidopsis
but larger than in rice which contains only three genes. The B3 subgoup
includes four genes in coffee while this subgroup contains only one member in
Arabidopsis as well as in rice. At the opposite, two subgroups (B2 and B4)
contain only one member each in coffee when they include three genes in
Arabidopsis. These data suggest different evolution of PSII LHCs between
coffee and Arabidopsis. In addition, the phylogenetic tree suggests a common
ancestor of multiple genomic loci each PSII subgroups before speciation
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between monocotyledons and dicotyledons. This subgroup expansion results
from gene duplication events taking place in each species, A. thaliana, rice and
coffee.
Furthermore, three additional LHC related genes were identified in coffee
genome, likely in A.thaliana and rice. Their amino acid sequences are relatively
conserved between three plants, A. thaliana, rice and coffee. Coffee CcPsbS is
ortholog of Arabidopsis PsbS (At1G44575) and two rice PsbSs
(LOC_Os01g64960 and LOC_Os04g59440). In Arabidopsis, PsbS protein,
subunit of photosystem II, plays a key role in nonphotochemical quenching
function in the regulation of photosynthetic light harvesting. This protein is
needed for photoprotective thermal dissipation of excess absorbed light energy
in plants (Niyogi et al., 2005). At the amino acid level, the homology is quite
high between orthologs: the CcPsbS sequence of 274 amino acids exhibits 72
/79 % of identity/similarity with AtPsbS,75/82% and 73/79% with OsPsbS1
and OsPsbS2, respectively.
The CcChla/b-like deduced protein shows similarity level of 75/90% for
285 amino acids with F14G6.17 (At1G76570) of A. thaliana and of 75/87%
for 281 amino acids with rice Chl a/b (LOC_Os09g12540), respectively. While
CcLIL is ortholog of Arabidopsis LIL3:1 (At4G17600, homology level at
%63/74 for 218 amino acids) and rice LIL (LoC_os02g03330, homology level
at %79/89 for 158 amino acids). However, any ortholog of Arabidopsis
F21B23.110 (AT5G28450), another chlorophyll a/b-binding protein was found
in coffee genome.
2553
Figure 1. Phylogenetic tree of the LHC family from A. thaliana (At), rice (Os) and coffee (Cc).
The tree was generated using Mega 5 program by Maximum Likelihood method. Bootstrap
values are indicated at each branch.
In coffee genome, five light-inducible genes have been isolated in
contrast to the six and eleven orthologs reported in genome of A. thaliana and
rice, respectively (Umate, 2010). Among them, two one-helix proteins (CcOHP
and CcOHP2) are orthologs of high light-inducible protein. Two two-helices
(CcSEP1 and CcSEP2) are orthologs of stress-enhanced proteins. These four
proteins do not contain typical Chloroa_b-bind (PF00504) conserved domain.
But they are relatively identical to OHP and SEP of other plants at the amino
acid level. CcOHP exhibits 74/86% of identity/positif for 81 amino acids with
AtOHP (At5G02120) and 81/91% for 74 amino acids with OsOHP1
(LOC_os05g2273). While CcOHP2 shows similarity level of 67/73%
(identities/positives) for 153 amino acids with AtOHP2 (At1G34000) and
56/65% for 170 amino acids with rice OsOHP2 (LOC_os01g40710). The
protein alignment of OHPs in rice, Arabidopsis and coffee is presented in figure
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2. Similarly, CcSEP1 shares similarity level of 55/71% for 144 amino acids
with Arabidopsis SEP1 (At4G34190) when CcSEP2 shows similarity level of
60/75% for 162 amino acids with Arabidopsis SEP2 (At2G21970) and 51/68%
for 166 amino acids with rice OsSEP2 (LOC_Os04g54630). The full-length
amino acid aligment of SEPs in rice, A.thaliana and coffee is shown in figure 3.
The remaining, ortholog of early light-inducible proteins of A.thaliana and rice,
was named as CcELIP. At amino acid level, CcELIP shares homology of
60/73% 191 amino acid with tea ELIP2 (genbank accession FE942102) and
%51/66% with Arabidopsis ELIP2 (At4G14690). The full-length amino acid
aligment of ELIP in rice, Tortula ruralis, A.thaliana, tea and coffee is shown in
figure 4.
Figure 2. Full-length amino acid alignment of OHP proteins in rice (Os), Arabidopsis thaliana
(At) and Coffee (Cc) by using MAFFT. Asterisks and dots drawn on bottom of sequence
indicate identical residues and conservative amino acid changes, respectively. Helix motif is
noted by line on top.
Figure3. Full-length amino acid alignment of SEP proteins in rice (Os), Arabidopsis thaliana
(At) and Coffee (Cc) by using MAFFT. Asterisks and dots drawn on bottom of sequence
indicate identical residues and conservative amino acid changes, respectively. Helix motifs are
noted by line on top.
2555
Figure 4. Full-length amino acid alignment of ELIP proteins in Tortula ruralis (Tr), rice (Os),
Arabidopsis thaliana (At), thea (Cs), and Coffee (Cc) by using MAFFT. Asterisks and dots
drawn on bottom of sequence indicate identical residues and conservative amino acid changes,
respectively. Helix motifs are noted by line on top.
Expression of coffee LHC genes
The expression of the LHC genes was analyzed via the in silico analyses
from transcriptome (RNAseq) data of coffee (C. canephora) tissues (Denoeud
et al., 2014). Expression analysis was performed on endosperm, perisperm,
leaf, pistil, stamen, and root. These data indicate that most of the coffee LHC
genes are strongly expressed in leaf and perisperm tissues while their
expression level is weakest in rootcompared to all investigated tissues. Among
the PSI LHC genes (A1-A6), CcLHCA5 is the less expressed in all analyzed
tissues. The other genes are highly expressed in leaves and perisperm, while
they are more weakly expressed in endosperm, roots, pistil and stamen.
Highest expression level was observed for CcLHCA1 gene in leaf and stamen,
for CcLHCA2 and CcLHCA4 in endosperm and perisperm. In addition,
CcLHCA4 is the most strongly expressed gene in pistil while CcLHCA3 is the
most strongly expressed in root.
Among the PSII LHC genes, single locus genes are expressed in all
examined tissues, except in roots where the expression of CcLHCB2 gene is
very weak. These genes are the most expressed in leaves and perisperm and the
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Journal of Agricultural Technology 2015 Vol. 11(8): 2547-2561
less expressed in roots. High expression levels are observed in pistil for these
four genes. The expression of multiple genomic loci genes varies. Only three
members of B1 subgroup (CcLHCB1.3-CcLHC1.5) are expressed in most of
investigated tissues while the expression of two remaining genes is very weak
or not detected. Similarly, CcLHCB4.3 was unique gene of B4 subgroup
expressed in all studied tissues. To date, the expression of PSI and LHC genes
is little known in plants, especially in normal conditions. Nicotiana sylvestris
Lhcb1 transcripts are accumulated in leaves and stems but not in roots and
non-green cultured cells (Hasegawaet al., 2002). In general, expression of the
LHCB genes is regulated by multiple environmental and developmental factors
(for review, see Xu et al., 2012).
The expression of three LHC-related genes is detected in various tissues
with highest expression in leaf and perisperm. CcChla/b-like and CcLIL genes
expressed in all tissues. LIL gene was known to play important role in the
chlorophyll and tocopherol biosynthesis in A.thaliana (Tanaka et al., 2010).
The expression of CcPsbS, subunit of PSII complex, was oberved in leaf,
perisperm, pistil and stamen. Arabidopsis orthologs play a key role in
nonphotochemical quenching function in the regulation of photosynthetic light
harvesting. This protein is important for photoprotective thermal dissipation of
excessive absorbed light energy in plants (Niyogi et al., 2005). Expression of
PsbS gene was responsive to high light in Arabidopsis (Li et al., 2000). While
psbS transcription seems to be influenced only by phytochrome and not by the
blue light low fluence system in spinach (Adamska et al., 1996). Recently,
accumulation of PsbS transcrits under various cadmium concentrations was
reported in Sedum alfredii ecotypes (Zhang and Yang, 2014).
The expression of light-inducible genes have been detected in all tissues.
In particular, CcELIP gene strongly expressed in leaves, endosperm, perisperm,
stamen and pistil. Interestingly, this gene is highly expressed in pistil, a
reproductive tissu. The expression of light-inducible genes is most studied
among LHC and LHC-related genes in other plants. Light-stress induced the
expression of OHP, SEP and ELIP genes in many plants, such as A. thaliana
OHP (Andersson et al., 2003; Heddad and Adamska, 2000; Heddad et al.,
2006). The expression of ELIP genes is induced by many abiotic stress
including cold, drought, high temperature and salinity in other plants (Adamska
and Kloppstech, 1994; Berti and Pinto, 2012; Montane and Kloppstech, 2000;
Peng et al., 2008; Wang et al., 2014). In addition, expression of ELIPs were
influenced by developmental stage of pea (NorÉN et al., 2003) and leaf
senescence of Nicotiana tabacum (Binyamin et al., 2001). In this work, the
expression of LHC genes in coffee under normal condition was reported,
suggesting that these genes play a constitutive role in both vegetative and
2557
reproductive tissues of this plant.
Figure 5. Heatmap showing expression level of coffee LHC genes in six organs. Color scale
represents RPKM normalized log10 transformed counts. Light red indicates low expression and
red indicates high expression.
Conclusion
By using in silico methods, a total of 28 putative LHC encoding genes
were found in coffee (Coffea cenaphora) genome. Twenty-three out of twentyeight putative LHC deduced proteins exhibit the Chloroa_b-bind (PF00504)
conserved domain. Based on phylogeny analysis, these coffee LHC genes were
classified into many groups, including PSI (six genes), PSII (14 genes), LHCrelated genes (three genes) and light-inducible genes (five genes). The PSI LHC
genes were divided into six subgroups (A1-A6) similarly to the PSII LHC
genes (B1-B6). In agreement to the situation in rice and A.thaliana, the B5 and
B6 subgroup include one gene each while B1 subgroup contains muliple
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genomic loci (five members). In adverse, B2 and B4 are single locus subgroup
in coffee but they are multiple genomic loci in both A. thaliana and rice.
However, B3 subgroup contains four genes in coffee but this subgroup has only
one member in A. thaliana. In general, the transcript of most of coffee putative
LHC genes were strongly detected in leaves and perisperm but weakly or no
detected in roots. In addition, most of these genes are expressed in pistil. The
coffee early light-inducible protein encoding gene strongly expressed in all
examinaed tissues.
List of abbreviations
CAB: chlorophyll a/b-binding protein; ELIP: early light-induced protein;
EST: expressed sequence tag; HLIP: high light-induced protein; LHC: lightharvesting complex; SEP: stress-enhanced proteins;
Acknowledgments
This work was funded by fundamental research programme of Hung
Vuong University. We acknowledge Pr C. Teulières and Dr C. Marques from
Paul Sabatier University (France) for critical reviewing of the manuscript and
English editing.
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